Neuroimmune Crosstalk through Extracellular Vesicles in Health and Disease

Trends in Neurosciences - Tập 42 - Trang 361-372 - 2019
Jean-Christophe Delpech1, Shawn Herron1, Mina B. Botros1, Tsuneya Ikezu1,2
1Department of Pharmacology and Experimental Therapeutics, Boston University School of Medicine, Boston, MA 02118 USA
2Neurology, Boston University School of Medicine, Boston, MA 02118, USA

Tài liệu tham khảo

Graner, 2009, Proteomic and immunologic analyses of brain tumor exosomes, FASEB J., 23, 1541, 10.1096/fj.08-122184 Shi, 2016, CNS tau efflux via exosomes is likely increased in Parkinson’s disease but not in Alzheimer’s disease, Alzheimers Dement., 12, 1125, 10.1016/j.jalz.2016.04.003 Mustapic, 2017, Plasma extracellular vesicles enriched for neuronal origin: a potential window into brain pathologic processes, Front. Neurosci., 11, 278, 10.3389/fnins.2017.00278 Sardar Sinha, 2018, Alzheimer’s disease pathology propagation by exosomes containing toxic amyloid-beta oligomers, Acta Neuropathol., 136, 41, 10.1007/s00401-018-1868-1 Joshi, 2014, Microglia convert aggregated amyloid-β into neurotoxic forms through the shedding of microvesicles, Cell Death Differ., 21, 582, 10.1038/cdd.2013.180 Saman, 2012, Exosome-associated tau is secreted in tauopathy models and is selectively phosphorylated in cerebrospinal fluid in early Alzheimer disease, J. Biol. Chem., 287, 3842, 10.1074/jbc.M111.277061 Colombo, 2014, Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles, Annu. Rev. Cell Dev. Biol., 30, 255, 10.1146/annurev-cellbio-101512-122326 Thery, 2002, Exosomes: composition, biogenesis and function, Nat. Rev. Immunol., 2, 569, 10.1038/nri855 Zhang, 2015, Exosome and exosomal microRNA: trafficking, sorting, and function, Genomics Proteomics Bioinformatics, 13, 17, 10.1016/j.gpb.2015.02.001 Nazarenko, 2010, Cell surface tetraspanin Tspan8 contributes to molecular pathways of exosome-induced endothelial cell activation, Cancer Res., 70, 1668, 10.1158/0008-5472.CAN-09-2470 Eldh, 2010, Exosomes communicate protective messages during oxidative stress; possible role of exosomal shuttle RNA, PLoS One, 5, 10.1371/journal.pone.0015353 Carayon, 2011, Proteolipidic composition of exosomes changes during reticulocyte maturation, J. Biol. Chem., 286, 34426, 10.1074/jbc.M111.257444 de Jong, 2012, Cellular stress conditions are reflected in the protein and RNA content of endothelial cell-derived exosomes, J. Extracell. Vesicles, 1, 18396, 10.3402/jev.v1i0.18396 Pusic, 2014, Youth and environmental enrichment generate serum exosomes containing miR-219 that promote CNS myelination, Glia, 62, 284, 10.1002/glia.22606 Fitzner, 2011, Selective transfer of exosomes from oligodendrocytes to microglia by macropinocytosis, J. Cell Sci., 124, 447, 10.1242/jcs.074088 Kramer-Albers, 2007, Oligodendrocytes secrete exosomes containing major myelin and stress-protective proteins: trophic support for axons?, Proteomics Clin. Appl., 1, 1446, 10.1002/prca.200700522 Antonucci, 2012, Microvesicles released from microglia stimulate synaptic activity via enhanced sphingolipid metabolism, EMBO J., 31, 1231, 10.1038/emboj.2011.489 Ciregia, 2017, Extracellular vesicles in brain tumors and neurodegenerative diseases, Front. Mol. Neurosci., 10, 276, 10.3389/fnmol.2017.00276 Robbins, 2017, Extracellular vesicles and aging, Stem Cell Investig., 4, 98, 10.21037/sci.2017.12.03 Szepesi, 2018, Bidirectional microglia–neuron communication in health and disease, Front. Cell. Neurosci., 12, 323, 10.3389/fncel.2018.00323 Eyo, 2013, Bidirectional microglia-neuron communication in the healthy brain, Neural Plast., 2013, 456857, 10.1155/2013/456857 Biber, 2007, Neuronal ‘On’ and ‘Off’ signals control microglia, Trends Neurosci., 30, 596, 10.1016/j.tins.2007.08.007 Caruso, 2018, Apoptotic cell-derived extracellular vesicles: more than just debris, Front. Immunol., 9, 1486, 10.3389/fimmu.2018.01486 Butovsky, 2014, Identification of a unique TGF-β-dependent molecular and functional signature in microglia, Nat. Neurosci., 17, 131, 10.1038/nn.3599 Weber, 2015, Osteopontin mediates an MZF1-TGF-β1-dependent transformation of mesenchymal stem cells into cancer-associated fibroblasts in breast cancer, Oncogene, 34, 4821, 10.1038/onc.2014.410 Matias, 2018, Microglia/astrocytes–glioblastoma crosstalk: crucial molecular mechanisms and microenvironmental factors, Front. Cell. Neurosci., 12, 235, 10.3389/fncel.2018.00235 Fitzgerald, 2018, A system of cytokines encapsulated in extracellular vesicles, Sci. Rep., 8, 10.1038/s41598-018-27190-x Bianco, 2005, Astrocyte-derived ATP induces vesicle shedding and IL-1β release from microglia, J. Immunol., 174, 7268, 10.4049/jimmunol.174.11.7268 Drago, 2017, ATP modifies the proteome of extracellular vesicles released by microglia and influences their action on astrocytes, Front. Pharmacol., 8, 910, 10.3389/fphar.2017.00910 Kumar, 2017, Microglial-derived microparticles mediate neuroinflammation after traumatic brain injury, J. Neuroinflammation, 14, 47, 10.1186/s12974-017-0819-4 Yang, 2018, Inflammation leads to distinct populations of extracellular vesicles from microglia, J. Neuroinflammation, 15, 168, 10.1186/s12974-018-1204-7 Verderio, 2012, Myeloid microvesicles are a marker and therapeutic target for neuroinflammation, Ann. Neurol., 72, 610, 10.1002/ana.23627 Takenouchi, 2015, Extracellular ATP induces unconventional release of glyceraldehyde-3-phosphate dehydrogenase from microglial cells, Immunol. Lett., 167, 116, 10.1016/j.imlet.2015.08.002 Li, 2018, In vivo evidence for the contribution of peripheral circulating inflammatory exosomes to neuroinflammation, J. Neuroinflammation, 15, 8, 10.1186/s12974-017-1038-8 Théry, 2018, Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines, J. Extracell. Vesicles, 7, 10.1080/20013078.2018.1535750 Kanninen, 2016, Exosomes as new diagnostic tools in CNS diseases, Biochim. Biophys. Acta, 1862, 403, 10.1016/j.bbadis.2015.09.020 Matsumoto, 2017, The transport mechanism of extracellular vesicles at the blood-brain barrier, Curr. Pharm. Des., 23, 6206, 10.2174/1381612823666170913164738 Lachenal, 2011, Release of exosomes from differentiated neurons and its regulation by synaptic glutamatergic activity, Mol. Cell. Neurosci., 46, 409, 10.1016/j.mcn.2010.11.004 Budnik, 2016, Extracellular vesicles round off communication in the nervous system, Nat. Rev. Neurosci., 17, 160, 10.1038/nrn.2015.29 Fruhbeis, 2013, Neurotransmitter-triggered transfer of exosomes mediates oligodendrocyte-neuron communication, PLoS Biol., 11, 10.1371/journal.pbio.1001604 Goldie, 2014, Activity-associated miRNA are packaged in Map1b-enriched exosomes released from depolarized neurons, Nucleic Acids Res., 42, 9195, 10.1093/nar/gku594 Morel, 2013, Neuronal exosomal miRNA-dependent translational regulation of astroglial glutamate transporter GLT1, J. Biol. Chem., 288, 7105, 10.1074/jbc.M112.410944 Bahrini, 2015, Neuronal exosomes facilitate synaptic pruning by up-regulating complement factors in microglia, Sci. Rep., 5, 10.1038/srep07989 Fruhbeis, 2012, Emerging roles of exosomes in neuron-glia communication, Front. Physiol., 3, 119, 10.3389/fphys.2012.00119 Frohlich, 2014, Multifaceted effects of oligodendroglial exosomes on neurons: impact on neuronal firing rate, signal transduction and gene regulation, Philos. Trans. R. Soc. Lond. B Biol. Sci., 369, 10.1098/rstb.2013.0510 Kocur, 2015, IFNβ secreted by microglia mediates clearance of myelin debris in CNS autoimmunity, Acta Neuropathol. Commun., 3, 20, 10.1186/s40478-015-0192-4 Lampron, 2015, Inefficient clearance of myelin debris by microglia impairs remyelinating processes, J. Exp. Med., 212, 481, 10.1084/jem.20141656 Paolicelli, 2019, Cell-to-cell communication by extracellular vesicles: focus on microglia, Neuroscience, 10.1016/j.neuroscience.2018.04.003 Potolicchio, 2005, Proteomic analysis of microglia-derived exosomes: metabolic role of the aminopeptidase CD13 in neuropeptide catabolism, J. Immunol., 175, 2237, 10.4049/jimmunol.175.4.2237 Prada, 2018, Glia-to-neuron transfer of miRNAs via extracellular vesicles: a new mechanism underlying inflammation-induced synaptic alterations, Acta Neuropathol., 135, 529, 10.1007/s00401-017-1803-x Taylor, 2007, Regulation of heat shock protein 70 release in astrocytes: role of signaling kinases, Dev. Neurobiol., 67, 1815, 10.1002/dneu.20559 Proia, 2008, Astrocytes shed extracellular vesicles that contain fibroblast growth factor-2 and vascular endothelial growth factor, Int. J. Mol. Med., 21, 63 Wang, 2011, Synapsin I is an oligomannose-carrying glycoprotein, acts as an oligomannose-binding lectin, and promotes neurite outgrowth and neuronal survival when released via glia-derived exosomes, J. Neurosci., 31, 7275, 10.1523/JNEUROSCI.6476-10.2011 DeLeo, 2018, Extracellular vesicle biology in Alzheimer’s disease and related tauopathy, J. Neuroimmune Pharmacol., 13, 292, 10.1007/s11481-017-9768-z Yuyama, 2015, A potential function for neuronal exosomes: sequestering intracerebral amyloid-β peptide, FEBS Lett., 589, 84, 10.1016/j.febslet.2014.11.027 Yuyama, 2016, Physiological and pathological roles of exosomes in the nervous system, Biomol. Concepts, 7, 53, 10.1515/bmc-2015-0033 Yuyama, 2017, Exosomes as carriers of Alzheimer’s amyloid-β, Front. Neurosci., 11, 229, 10.3389/fnins.2017.00229 Rajendran, 2006, Alzheimer’s disease β-amyloid peptides are released in association with exosomes, Proc. Natl. Acad. Sci. U. S. A., 103, 11172, 10.1073/pnas.0603838103 Fiandaca, 2015, Identification of preclinical Alzheimer’s disease by a profile of pathogenic proteins in neurally derived blood exosomes: a case-control study, Alzheimers Dement., 11, 600, 10.1016/j.jalz.2014.06.008 Dinkins, 2014, Exosome reduction in vivo is associated with lower amyloid plaque load in the 5XFAD mouse model of Alzheimer’s disease, Neurobiol. Aging, 35, 1792, 10.1016/j.neurobiolaging.2014.02.012 Asai, 2015, Depletion of microglia and inhibition of exosome synthesis halt tau propagation, Nat. Neurosci., 18, 1584, 10.1038/nn.4132 Yuyama, 2012, Sphingolipid-modulated exosome secretion promotes clearance of amyloid-β by microglia, J. Biol. Chem., 287, 10977, 10.1074/jbc.M111.324616 Gouwens, 2018, Aβ42 protofibrils interact with and are trafficked through microglial-derived microvesicles, ACS Chem. Neurosci., 9, 1416, 10.1021/acschemneuro.8b00029 Eitan, 2016, Extracellular vesicle-associated Aβ mediates trans-neuronal bioenergetic and Ca2+-handling deficits in Alzheimer’s disease models, NPJ Aging Mech. Dis., 2, 16019, 10.1038/npjamd.2016.19 Goetzl, 2016, Cargo proteins of plasma astrocyte-derived exosomes in Alzheimer’s disease, FASEB J., 30, 3853, 10.1096/fj.201600756R Polanco, 2016, Extracellular vesicles isolated from the brains of rTg4510 mice seed tau protein aggregation in a threshold-dependent manner, J. Biol. Chem., 291, 12445, 10.1074/jbc.M115.709485 Wang, 2017, The release and trans-synaptic transmission of Tau via exosomes, Mol. Neurodegener., 12, 5, 10.1186/s13024-016-0143-y Medina, 2014, The role of extracellular Tau in the spreading of neurofibrillary pathology, Front. Cell. Neurosci., 8, 113, 10.3389/fncel.2014.00113 Agosta, 2014, Myeloid microvesicles in cerebrospinal fluid are associated with myelin damage and neuronal loss in mild cognitive impairment and Alzheimer disease, Ann. Neurol., 76, 813, 10.1002/ana.24235 Clayton, 2017, Alzheimer’s disease: the role of microglia in brain homeostasis and proteopathy, Front. Neurosci., 11, 680, 10.3389/fnins.2017.00680 El Andaloussi, 2013, Extracellular vesicles: biology and emerging therapeutic opportunities, Nat. Rev. Drug Discov., 12, 347, 10.1038/nrd3978 Raposo, 2013, Extracellular vesicles: exosomes, microvesicles, and friends, J. Cell Biol., 200, 373, 10.1083/jcb.201211138 Gyorgy, 2011, Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles, Cell. Mol. Life Sci., 68, 2667, 10.1007/s00018-011-0689-3 Andreu, 2014, Tetraspanins in extracellular vesicle formation and function, Front. Immunol., 5, 442, 10.3389/fimmu.2014.00442 Abels, 2016, Introduction to extracellular vesicles: biogenesis, RNA cargo selection, content, release, and uptake, Cell. Mol. Neurobiol., 36, 301, 10.1007/s10571-016-0366-z Mulcahy, 2014, Routes and mechanisms of extracellular vesicle uptake, J. Extracell. Vesicles, 3, 24641, 10.3402/jev.v3.24641 Grad, 2015, From molecule to molecule and cell to cell: prion-like mechanisms in amyotrophic lateral sclerosis, Neurobiol. Dis., 77, 257, 10.1016/j.nbd.2015.02.009 Basso, 2013, Mutant copper-zinc superoxide dismutase (SOD1) induces protein secretion pathway alterations and exosome release in astrocytes: implications for disease spreading and motor neuron pathology in amyotrophic lateral sclerosis, J. Biol. Chem., 288, 15699, 10.1074/jbc.M112.425066 Ferrara, 2018, Role of extracellular vesicles in amyotrophic lateral sclerosis, Front. Neurosci., 12, 574, 10.3389/fnins.2018.00574 Zhang, 2016, Potential transfer of polyglutamine and CAG-repeat RNA in extracellular vesicles in Huntington’s disease: background and evaluation in cell culture, Cell. Mol. Neurobiol., 36, 459, 10.1007/s10571-016-0350-7 Saenz-Cuesta, 2014, Extracellular vesicles in multiple sclerosis: what are they telling us?, Front. Cell. Neurosci., 8, 100, 10.3389/fncel.2014.00100 Minagar, 2003, Blood-brain barrier disruption in multiple sclerosis, Mult. Scler., 9, 540, 10.1191/1352458503ms965oa Prada, 2013, Classical and unconventional pathways of vesicular release in microglia, Glia, 61, 1003, 10.1002/glia.22497 Shi, 2014, Plasma exosomal α-synuclein is likely CNS-derived and increased in Parkinson’s disease, Acta Neuropathol., 128, 639, 10.1007/s00401-014-1314-y Danzer, 2012, Exosomal cell-to-cell transmission of alpha synuclein oligomers, Mol. Neurodegener., 7, 42, 10.1186/1750-1326-7-42 Fevrier, 2004, Cells release prions in association with exosomes, Proc. Natl. Acad. Sci. U. S. A., 101, 9683, 10.1073/pnas.0308413101 Bellingham, 2012, Small RNA deep sequencing reveals a distinct miRNA signature released in exosomes from prion-infected neuronal cells, Nucleic Acids Res., 40, 10937, 10.1093/nar/gks832 McKee, 2013, The spectrum of disease in chronic traumatic encephalopathy, Brain, 136, 43, 10.1093/brain/aws307 Stern, 2016, Preliminary study of plasma exosomal tau as a potential biomarker for chronic traumatic encephalopathy, J. Alzheimers Dis., 51, 1099, 10.3233/JAD-151028